1.1-billion-year-old porphyrins establish a marine ecosystem dominated by bacterial primary producers

Abstract

The average cell size of marine phytoplankton is critical for the flow of energy and nutrients from the base of the food web to higher trophic levels. Thus, the evolutionary succession of primary producers through Earth's history is important for our understanding of the radiation of modern protists ∼800 million years ago and the emergence of eumetazoan animals ∼200 million years later. Currently, it is difficult to establish connections between primary production and the proliferation of large and complex organisms because the mid-Proterozoic (∼1,800-800 million years ago) rock record is nearly devoid of recognizable phytoplankton fossils. We report the discovery of intact porphyrins, the molecular fossils of chlorophylls, from 1,100-million-year-old marine black shales of the Taoudeni Basin (Mauritania), 600 million years older than previous findings. The porphyrin nitrogen isotopes (δN = 5.6-10.2‰) are heavier than in younger sedimentary sequences, and the isotopic offset between sedimentary bulk nitrogen and porphyrins (ε = -5.1 to -0.5‰) points to cyanobacteria as dominant primary producers. Based on fossil carotenoids, anoxygenic green (Chlorobiacea) and purple sulfur bacteria (Chromatiaceae) also contributed to photosynthate. The low ε values, in combination with a lack of diagnostic eukaryotic steranes in the time interval of 1,600-1,000 million years ago, demonstrate that algae played an insignificant role in mid-Proterozoic oceans. The paucity of algae and the small cell size of bacterial phytoplankton may have curtailed the flow of energy to higher trophic levels, potentially contributing to a diminished evolutionary pace toward complex eukaryotic ecosystems and large and active organisms.

Microbial assemblage and palaeoenvironmental reconstruction of the 1.38 Ga Velkerri Formation, McArthur Basin, northern Australia

“…The genuine absence or low concentration of TMAI in the Velkerri Formation is important because it distinguishes its environment from other Proterozoic formations such as the Barney Creek Formation (Brocks et al., ) and the 1.1 Ga El Mreïti Group (Gueneli et al., ). We therefore investigate whether the extremely low concentrations of TMAI reflect primary absence or are due to thermal breakdown or oxygen exposure during degradation.…”

“…These geochemical conditions and biomarker assemblages are broadly comparable to black, finely laminated shales from the ca . 1.1 Ga El Mreïti Group in the Taoudeni Basin, Mauritania (Blumenberg et al., ; Gueneli et al., ). There, the presence of 2,3,4‐ and 2,3,6‐TMAI, in addition to iron speciation, and sulphur isotopes of pyrite and redox‐sensitive trace elements all suggest nearshore PZE conditions (Blumenberg et al., ; Gilleaudeau & Kah, ; Gueneli et al., ; Kah, Bartley, & Teal, ).…”

“…1.1 Ga El Mreïti Group in the Taoudeni Basin, Mauritania (Blumenberg et al., ; Gueneli et al., ). There, the presence of 2,3,4‐ and 2,3,6‐TMAI, in addition to iron speciation, and sulphur isotopes of pyrite and redox‐sensitive trace elements all suggest nearshore PZE conditions (Blumenberg et al., ; Gilleaudeau & Kah, ; Gueneli et al., ; Kah, Bartley, & Teal, ). Moreover, the nitrogen isotopic composition of porphyrins from the El Mreïti Group confirms that primary productivity was dominated by bacteria (Gueneli et al., ), and there is no fossil (Beghin, Guilbaud, et al., ; Beghin, Storme, et al., ) or biomarker evidence for the activity of algae (Blumenberg et al., ; Gueneli et al., ).…”

“…There, the presence of 2,3,4‐ and 2,3,6‐TMAI, in addition to iron speciation, and sulphur isotopes of pyrite and redox‐sensitive trace elements all suggest nearshore PZE conditions (Blumenberg et al., ; Gilleaudeau & Kah, ; Gueneli et al., ; Kah, Bartley, & Teal, ). Moreover, the nitrogen isotopic composition of porphyrins from the El Mreïti Group confirms that primary productivity was dominated by bacteria (Gueneli et al., ), and there is no fossil (Beghin, Guilbaud, et al., ; Beghin, Storme, et al., ) or biomarker evidence for the activity of algae (Blumenberg et al., ; Gueneli et al., ). Thus, the combination of these studies, in addition to trace metal redox work in other locations, suggests environmental heterogeneity in the Mesoproterozoic (e.g., Canfield, ; Lyons, Anbar, Severmann, Scott, & Gill, ).…”

Exploring cycad foliage as an archive of the isotopic composition of atmospheric nitrogen

“…More recently, Silverman, Kopf, Bebout, Gordon, and Som (2019) showed that the nitrogen isotopic fractionation during N 2 fixation changes as a function of pN 2 in some species of cyanobacteria. As microbial N 2 fixation is thought to have arisen early in Earth's history (Stüeken, Buick, Guy, & Koehler, 2015;Weiss et al, 2016) and cyanobacteria may have dominated primary productivity through much of the Precambrian (Brocks et al, 2017;Gueneli et al, 2018), they could perhaps provide a long-term record of both pN 2 and the δ 15 N of atmospheric N 2 . However, because δ 15 N values of bulk marine sediments can be altered by a few permil during diagenesis (Robinson et al, 2012) and represent a mixture of biomass from N 2 -fixing and non-N 2 -fixing organisms, this would require the nitrogen isotopic analysis of discrete cyanobacterial fossils instead of bulk marine sediments.…”